Broad functional profiling of fission yeast proteins using phenomics and machine learning
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Abstract
Many proteins remain poorly characterized even in well-studied organisms, presenting a bottleneck for research. We applied phenomics and machine-learning approaches with Schizosaccharomyces pombe for broad cues on protein functions. We assayed colony-growth phenotypes to measure the fitness of deletion mutants for 3509 non-essential genes in 131 conditions with different nutrients, drugs, and stresses. These analyses exposed phenotypes for 3492 mutants, including 124 mutants of ‘priority unstudied’ proteins conserved in humans, providing varied functional clues. For example, over 900 proteins were newly implicated in the resistance to oxidative stress. Phenotype-correlation networks suggested roles for poorly characterized proteins through ‘guilt by association’ with known proteins. For complementary functional insights, we predicted Gene Ontology (GO) terms using machine learning methods exploiting protein-network and protein-homology data (NET-FF). We obtained 56,594 high-scoring GO predictions, of which 22,060 also featured high information content. Our phenotype-correlation data and NET-FF predictions showed a strong concordance with existing PomBase GO annotations and protein networks, with integrated analyses revealing 1675 novel GO predictions for 783 genes, including 47 predictions for 23 priority unstudied proteins. Experimental validation identified new proteins involved in cellular aging, showing that these predictions and phenomics data provide a rich resource to uncover new protein functions.
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Cites
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1131 · Cited by 17,749 · see citing works
Metascape provides a biologist-oriented resource for the analysis of systems-level datasets
Zhou, Y., Zhou, B., Pache, L., Chang, M., Khodabakhshi, A. H., Tanaseichuk, O., Benner, C., & Chanda, S. K. (2019) · Nature Communications · doi:10.1038/s41467-019-09234-6 · Cited by 14,611 · see citing works
STRING v10: protein–protein interaction networks, integrated over the tree of life
Szklarczyk, D., Franceschini, A., Wyder, S., Forslund, K., Heller, D., Huerta-Cepas, J., Simonovic, M., Roth, A., Santos, A., Tsafou, K. P., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1003 · Cited by 10,436 · see citing works
Szklarczyk, D., Gable, A. L., Nastou, K. C., Lyon, D., Kirsch, R., Pyysalo, S., Doncheva, N. T., Legeay, M., Fang, T., Bork, P., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1074 · Cited by 8,056 · see citing works
UniProt: a worldwide hub of protein knowledge
The UniProt Consortium (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1049 · Cited by 7,698 · see citing works
Raudvere, U., Kolberg, L., Kuzmin, I., Arak, T., Adler, P., Peterson, H., & Vilo, J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz369 · Cited by 5,045 · see citing works
The Gene Ontology Resource: 20 years and still GOing strong
The Gene Ontology Consortium (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1055 · Cited by 4,747 · see citing works
The Pfam protein families database in 2019
El-Gebali, S., Mistry, J., Bateman, A., Eddy, S. R., Luciani, A., Potter, S. C., Qureshi, M., Richardson, L. J., Salazar, G. A., Smart, A., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gky995 · Cited by 4,602 · see citing works
Functional profiling of the Saccharomyces cerevisiae genome
Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., André, B., et al. (2002) · Nature · doi:10.1038/nature00935 · Cited by 4,316 · see citing works
The Gene Ontology resource: enriching a GOld mine
The Gene Ontology Consortium, Carbon, S., Douglass, E., Good, B. M., Unni, D. R., Harris, N. L., Mungall, C. J., Basu, S., Chisholm, R. L., Dodson, R. J., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1113 · Cited by 3,555 · see citing works
Self-citationMachine learning applications in genetics and genomics
Libbrecht, M. W., & Noble, W. S. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3920 · Cited by 2,142 · see citing works
The genome sequence of Schizosaccharomyces pombe
Wood, V., Gwilliam, R., Rajandream, M.-A., Lyne, M. H., Lyne, R., Stewart, A., SGOUROS, J. G., Peat, N., Hayles, J., Baker, S. G., et al. (2002) · Nature · doi:10.1038/nature724 · Cited by 1,650 · see citing works
Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions
Mistry, J., Finn, R. D., Eddy, S. R., Bateman, A. G., & Punta, M. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt263 · Cited by 1,622 · see citing works
Design and synthesis of a minimal bacterial genome
Hutchison, C. A., Chuang, R.-Y., Noskov, V. N., Assad-Garcia, N., Deerinck, T. J., Ellisman, M. H., Gill, J., Kannan, K., Karas, B. J., Ma, L., et al. (2016) · Science · doi:10.1126/science.aad6253 · Cited by 1,500 · see citing works
Deep learning for computational biology
Angermueller, C., Pärnamaa, T., Parts, L., & Stegle, O. (2016) · Molecular Systems Biology · doi:10.15252/msb.20156651 · Cited by 1,473 · see citing works
HH-suite3 for fast remote homology detection and deep protein annotation
Steinegger, M., Meier, M., Mirdita, M., Vöhringer, H., Haunsberger, S. J., & Söding, J. (2019) · BMC Bioinformatics · doi:10.1186/s12859-019-3019-7 · Cited by 1,145 · see citing works
A large-scale evaluation of computational protein function prediction
Radivojac, P., Clark, W. T., Oron, T. R., Schnoes, A. M., Wittkop, T., Sokolov, A., Graim, K., Funk, C., Verspoor, K., Ben-Hur, A., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2340 · Cited by 1,028 · see citing works
Self-citationThe Chemical Genomic Portrait of Yeast: Uncovering a Phenotype for All Genes
Hillenmeyer, M. E., Fung, E., Wildenhain, J., Pierce, S. E., Hoon, S. S., Lee, W., Proctor, M. J., St.Onge, R. P., Tyers, M., Koller, D., et al. (2008) · Science · doi:10.1126/science.1150021 · Cited by 978 · see citing works
The central role of DNA damage in the ageing process
Schumacher, B., Pothof, J., Vijg, J., & Hoeijmakers, J. H. J. (2021) · Nature · doi:10.1038/s41586-021-03307-7 · Cited by 907 · see citing works
Global transcriptional responses of fission yeast to environmental stress
Chen, D., Toone, W. M., Mata, J., Lyne, R., Burns, G., Kivinen, K., Brazma, A., Jones, N., & Bähler, J. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-08-0499 · Cited by 796 · see citing works
Self-citationAnalysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe
Kim, D.-U., Hayles, J., Kim, D., Wood, V., Park, H.-O., Won, M., Yoo, H.-S., Duhig, T., Nam, M., Palmer, G., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1628 · Cited by 742 · see citing works
clusterMaker: a multi-algorithm clustering plugin for Cytoscape
Morris, J. H., Apeltsin, L., Newman, A. M., Baumbach, J., Wittkop, T., Su, G., Bader, G. D., & Ferrin, T. E. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-436 · Cited by 609 · see citing works
Marguerat, S., Schmidt, A., Codlin, S., Chen, W., Aebersold, R., & Bähler, J. (2012) · Cell · doi:10.1016/j.cell.2012.09.019 · Cited by 571 · see citing works
Self-citationCATH: increased structural coverage of functional space
Sillitoe, I., Bordin, N., Dawson, N., Waman, V. P., Ashford, P., Scholes, H. M., Pang, C. S. M., Woodridge, L., Rauer, C., Sen, N., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1079 · Cited by 509 · see citing works
Self-citationThe transcriptional program of meiosis and sporulation in fission yeast
Mata, J., Lyne, R., Burns, G., & Bähler, J. (2002) · Nature Genetics · doi:10.1038/ng951 · Cited by 480 · see citing works
Self-citationZhou, N., Jiang, Y., Bergquist, T. R., Lee, A. J., Kacsoh, B. Z., Crocker, A. W., Lewis, K. A., Georghiou, G., Nguyen, H. N., Hamid, M. N., et al. (2019) · Genome Biology · doi:10.1186/s13059-019-1835-8 · Cited by 452 · see citing works
Self-citationMungall, C. J., McMurry, J. A., Köhler, S., Balhoff, J. P., Borromeo, C., Brush, M., Carbon, S., Conlin, T., Dunn, N., Engelstad, M., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1128 · Cited by 441 · see citing works
Edwards, A. M., Isserlin, R., Bader, G. D., Frye, S. V., Willson, T. M., & Yu, F. H. (2011) · Nature · doi:10.1038/470163a · Cited by 411 · see citing works
An expanded evaluation of protein function prediction methods shows an improvement in accuracy
Jiang, Y., Oron, T. R., Clark, W. T., Bankapur, A., D’Andrea, D., Lepore, R., Funk, C. S., Kahanda, I., Verspoor, K. M., Ben‐Hur, A., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1037-6 · Cited by 390 · see citing works
Self-citationStress-activated Genomic Expression Changes Serve a Preparative Role for Impending Stress in Yeast
Berry, D. B., & Gasch, A. P. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-07-0680 · Cited by 326 · see citing works
Erratum: Unexplored therapeutic opportunities in the human genome
Oprea, T. I., Bologa, C., Brunak, S., Campbell, A., Gan, G. N., Gaulton, A., Gomez, S. M., Guha, R., Hersey, A., Holmes, J., et al. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.52 · Cited by 304 · see citing works
Systematic discovery of nonobvious human disease models through orthologous phenotypes
McGary, K. L., Park, T. J., Woods, J. O., Ji, H. Y., Wallingford, J. B., & Marcotte, E. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910200107 · Cited by 292 · see citing works
Yeast signaling pathways in the oxidative stress response
Ikner, A., & Shiozaki, K. (2004) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2004.09.006 · Cited by 267 · see citing works
Large-scale investigation of the reasons why potentially important genes are ignored
Stoeger, T., Gerlach, M., Morimoto, R. I., & Nunes Amaral, L. A. (2018) · PLOS Biology · doi:10.1371/journal.pbio.2006643 · Cited by 261 · see citing works
An Ancient Yeast for Young Geneticists: A Primer on the Schizosaccharomyces pombe Model System
Hoffman, C. S., Wood, V., & Fantes, P. A. (2015) · Genetics · doi:10.1534/genetics.115.181503 · Cited by 238 · see citing works
deepNF: deep network fusion for protein function prediction
Gligorijević, V., Barot, M., & Bonneau, R. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty440 · Cited by 233 · see citing works
Comparing the performance of biomedical clustering methods
Wiwie, C., Baumbach, J., & Röttger, R. (2015) · Nature Methods · doi:10.1038/nmeth.3583 · Cited by 225 · see citing works
Multiple Pathways Differentially Regulate Global Oxidative Stress Responses in Fission Yeast
Chen, D., Wilkinson, C. R. M., Watt, S. B., Penkett, C. J., Toone, W. M., Jones, N., & Bähler, J. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-08-0735 · Cited by 209 · see citing works
Self-citationGene Ontology term overlap as a measure of gene functional similarity
Mistry, M., & Pavlidis, P. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-327 · Cited by 204 · see citing works
A Network of Multiple Regulatory Layers Shapes Gene Expression in Fission Yeast
Lackner, D. H., Beilharz, T. H., Marguerat, S., Mata, J., Watt, S., Schubert, F., Preiss, T., & Bähler, J. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.03.002 · Cited by 204 · see citing works
Self-citationGOLabeler: improving sequence-based large-scale protein function prediction by learning to rank
You, R., Zhang, Z., Xiong, Y., Sun, F., Mamitsuka, H., & Zhu, S. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty130 · Cited by 199 · see citing works
The proteome landscape of the kingdoms of life
Müller, J., Geyer, P. E., Colaço, A. R., Treit, P. V., Strauss, M. T., Oroshi, M., Doll, S., Winter, S. V., Bader, J. M., Köhler, N., et al. (2020) · Nature · doi:10.1038/s41586-020-2402-x · Cited by 199 · see citing works
ProteInfer, deep neural networks for protein functional inference
Sanderson, T., Bileschi, M. L., Belanger, D., & Colwell, L. J. (2023) · eLife · doi:10.7554/elife.80942 · Cited by 192 · see citing works
Gene annotation bias impedes biomedical research
Haynes, W. A., Tomczak, A., & Khatri, P. (2018) · Scientific Reports · doi:10.1038/s41598-018-19333-x · Cited by 192 · see citing works
Understudied proteins: opportunities and challenges for functional proteomics
Kustatscher, G., Collins, T., Gingras, A., Guo, T., Hermjakob, H., Ideker, T. E., Lilley, K. S., Lundberg, E. K., Marcotte, E. M., Ralser, M., et al. (2022) · Nature Methods · doi:10.1038/s41592-022-01454-x · Cited by 190 · see citing works
A genome-wide resource of cell cycle and cell shape genes of fission yeast
Hayles, J., Wood, V., Jeffery, L., Hoe, K., Kim, D.-U., Park, H.-O., Salas-Pino, S., Heichinger, C., & Nurse, P. (2013) · Open Biology · doi:10.1098/rsob.130053 · Cited by 171 · see citing works
Lock, A., Rutherford, K., Harris, M. A., Hayles, J., Oliver, S. G., Bähler, J., & Wood, V. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky961 · Cited by 165 · see citing works
Self-citationOMA standalone: orthology inference among public and custom genomes and transcriptomesPreprint
Altenhoff, A., Levy, J., Zarowiecki, M., Tomiczek, B., Vesztrocy, A. W., Dalquen, D. A., Müller, S., Telford, M. J., Glover, N. M., Dylus, D., et al. (2019) · Genome Research · doi:10.1101/gr.243212.118 · Cited by 159 · see citing works
Das, S., Lee, D., Sillitoe, I., Dawson, N. L., Lees, J. G., & Orengo, C. A. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv398 · Cited by 146 · see citing works
Self-citationRallis, C., Codlin, S., & Bähler, J. (2013) · Aging Cell · doi:10.1111/acel.12080 · Cited by 144 · see citing works
Self-citationHidden in plain sight: what remains to be discovered in the eukaryotic proteome?
Wood, V., Lock, A., Harris, M. A., Rutherford, K., Bähler, J., & Oliver, S. G. (2019) · Open Biology · doi:10.1098/rsob.180241 · Cited by 132 · see citing works
Self-citationOxidative stress in Schizosaccharomyces pombe: different H2O2 levels, different response pathways
Vivancos, A. P., Jara, M., Zuin, A., Sansó, M., & Hidalgo, E. (2006) · Molecular Genetics and Genomics · doi:10.1007/s00438-006-0175-z · Cited by 124 · see citing works
Mortensen, R. D., Serra, M., STEITZ, J. A., & Vasudevan, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105401108 · Cited by 124 · see citing works
Yao, S., You, R., Wang, S., Xiong, Y., Huang, X., & Zhu, S. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab398 · Cited by 119 · see citing works
GOGO: An improved algorithm to measure the semantic similarity between gene ontology terms
Zhao, C., & Wang, Z. (2018) · Scientific Reports · doi:10.1038/s41598-018-33219-y · Cited by 109 · see citing works
Zuin, A., Gabrielli, N., Calvo, I. A., García‐Santamarina, S., Hoe, K., Kim, D. U., Park, H.-O., Hayles, J., Ayté, J., & Hidalgo, E. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002842 · Cited by 106 · see citing works
Global Analysis of Fission Yeast Mating Genes Reveals New Autophagy Factors
Sun, L., Li, M., Suo, F., Liu, X., Shen, E.-Z., Yang, B., Dong, M., He, W., & Du, L. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003715 · Cited by 105 · see citing works
High-resolution network biology: connecting sequence with function
Ryan, C. J., Cimermančič, P., Szpiech, Z. A., Šali, A., Hernandez, R. D., & Krogan, N. J. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3574 · Cited by 98 · see citing works
A wealth of discovery built on the Human Genome Project — by the numbers
Gates, A. J., Gysi, D. M., Kellis, M., & Barabási, A.-L. (2021) · Nature · doi:10.1038/d41586-021-00314-6 · Cited by 98 · see citing works
Genome-Wide Screen of Genes Required for Caffeine Tolerance in Fission Yeast
Calvo, I. A., Gabrielli, N., Iglesias-Baena, I., García‐Santamarina, S., Hoe, K., Kim, D. U., Sansó, M., Zuin, A., Pérez, P., Ayté, J., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006619 · Cited by 88 · see citing works
AnGeLi: A Tool for the Analysis of Gene Lists from Fission Yeast
Bitton, D. A., Schubert, F., Dey, S., Okoniewski, M. J., Smith, G. C., Khadayate, S. P., Pancaldi, V., Wood, V., & Bähler, J. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00330 · Cited by 85 · see citing works
Self-citationSystematic Analysis of the Role of RNA-Binding Proteins in the Regulation of RNA Stability
Hasan, A., Cotobal, C., Duncan, C. D. S., & Mata, J. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004684 · Cited by 77 · see citing works
Rallis, C., López‐Maury, L., Georgescu, T. R., Pancaldi, V., & Bähler, J. (2014) · Biology Open · doi:10.1242/bio.20147245 · Cited by 69 · see citing works
Self-citationFYPO: the fission yeast phenotype ontology
Harris, M. A., Lock, A., Bähler, J., Oliver, S. G., & Wood, V. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt266 · Cited by 69 · see citing works
Self-citationPiazzon, N., Maisonneuve, C., Guilleret, I., Rotman, S., & Constam, D. B. (2012) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjs027 · Cited by 68 · see citing works
Deshpande, G., Hayles, J., Hoe, K., Kim, D.-U., Park, H.-O., & Hartsuiker, E. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.01.016 · Cited by 68 · see citing works
Temporal patterns of genes in scientific publications
Pfeiffer, T., & Hoffmann, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701315104 · Cited by 64 · see citing works
Brochado, A. R., & Typas, A. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.01.008 · Cited by 61 · see citing works
Duncan, C. D. S., Rodríguez‐López, M., Ruis, P., Bähler, J., & Mata, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713991115 · Cited by 61 · see citing works
Self-citationFunctional and regulatory profiling of energy metabolism in fission yeast
Małecki, M., Bitton, D. A., Rodríguez‐López, M., Rallis, C., Calavia, N. G., Smith, G. C., & Bähler, J. (2016) · Genome biology · doi:10.1186/s13059-016-1101-2 · Cited by 60 · see citing works
Self-citationSinha, S., Eisenhaber, B., Jensen, L. J., Kalbuaji, B., & Eisenhaber, F. (2018) · PROTEOMICS · doi:10.1002/pmic.201800093 · Cited by 60 · see citing works
cath-resolve-hits: a new tool that resolves domain matches suspiciously quickly
Lewis, T. E., Sillitoe, I., & Lees, J. G. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty863 · Cited by 57 · see citing works
Self-citationFission stories: Using PomBase to understand Schizosaccharomyces pombe biologyPreprint
Harris, M. A., Rutherford, K., Hayles, J., Lock, A., Bähler, J., Oliver, S. G., Mata, J., & Wood, V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.07.459264 · Cited by 57 · see citing works
Self-citationSideri, T. C., Rallis, C., Bitton, D. A., Lages, B. M., Suo, F., Rodríguez‐López, M., Du, L., & Bähler, J. (2014) · G3 Genes Genomes Genetics · doi:10.1534/g3.114.014415 · Cited by 55 · see citing works
Self-citationRodríguez‐López, M., Gonzalez, S., Hillson, O., Tunnacliffe, E., Codlin, S., Tallada, V. A., Bähler, J., & Rallis, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.058 · Cited by 55 · see citing works
Self-citationDudin, O., Merlini, L., Bendezú, F. O., Groux, R., Vincenzetti, V., & Martin, S. G. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006721 · Cited by 45 · see citing works
Pancaldi, V., Schubert, F., & Bähler, J. (2009) · Molecular BioSystems · doi:10.1039/b913876p · Cited by 44 · see citing works
Self-citationKamrad, S., Rodríguez‐López, M., Cotobal, C., Correia‐Melo, C., Ralser, M., & Bähler, J. (2020) · eLife · doi:10.7554/elife.55160 · Cited by 44 · see citing works
Self-citationHuttenhower, C., Hibbs, M., Myers, C. L., Caudy, A. A., Hess, D. C., & Troyanskaya, O. G. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp397 · Cited by 42 · see citing works
Gene2Function: An Integrated Online Resource for Gene Function Discovery
Hu, Y., Comjean, A., Mohr, S. E., Perrimon, N., Agapite, J., Broll, K., Crosby, M., Santos, G. D., Emmert, D., Falls, K., et al. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.043885 · Cited by 42 · see citing works
Power-law-like distributions in biomedical publications and research funding
Su, A. I., & Hogenesch, J. B. (2007) · Genome biology · doi:10.1186/gb-2007-8-4-404 · Cited by 41 · see citing works
Romila, C.-A., Townsend, S., Małecki, M., Kamrad, S., Rodríguez‐López, M., Hillson, O., Cotobal, C., Ralser, M., & Bähler, J. (2021) · Microbial Cell · doi:10.15698/mic2021.07.754 · Cited by 40 · see citing works
Self-citationA Novel Histone Deacetylase Complex in the Control of Transcription and Genome Stability
Zilio, N., Codlin, S., Vashisht, A. A., Bitton, D. A., Head, S. R., Wohlschlegel, J. A., Bähler, J., & Boddy, M. N. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00519-14 · Cited by 39 · see citing works
Self-citationGenetic regulation of mitotic competence in G 0 quiescent cells
Sajiki, K., Tahara, Y., Uehara, L., Sasaki, T., Pluskal, T., & Yanagida, M. (2018) · Science Advances · doi:10.1126/sciadv.aat5685 · Cited by 39 · see citing works
hsf1+ extends chronological lifespan through Ecl1 family genes in fission yeast
Ohtsuka, H., Azuma, K., Murakami, H., & Aiba, H. (2010) · Molecular Genetics and Genomics · doi:10.1007/s00438-010-0588-6 · Cited by 36 · see citing works
Global Fitness Profiling Identifies Arsenic and Cadmium Tolerance Mechanisms in Fission Yeast
Guo, L. P., Ganguly, A., Sun, L., Suo, F., Du, L., & Russell, P. R. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.033829 · Cited by 36 · see citing works
Identifying genes required for respiratory growth of fission yeast
Małecki, M., & Bähler, J. (2016) · Wellcome Open Research · doi:10.12688/wellcomeopenres.9992.1 · Cited by 28 · see citing works
Self-citationFunctional Genomics of Adhesion, Invasion, and Mycelial Formation in Schizosaccharomyces pombe
Dodgson, J., Avula, H., Hoe, K., Kim, D.-U., Park, H.-O., Hayles, J., & Armstrong, J. T. (2009) · Eukaryotic Cell · doi:10.1128/ec.00078-09 · Cited by 26 · see citing works
Lie, S., Banks, P., Lawless, C., Lydall, D. A., & Petersen, J. (2018) · Open Biology · doi:10.1098/rsob.180015 · Cited by 26 · see citing works
The CCR4-NOT Complex Is Implicated in the Viability of Aneuploid Yeasts
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Borao, S., Vega, M., Boronat, S., Hidalgo, E., Hümmer, S., & Ayté, J. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1011316
Piedade, W. P., Weeks, O., Moran, H. R., Akerberg, A. A., Molnar, M. M., Galdieri, J., Buick, A., Zheng, R., Chen, K., Keshishian, H., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.04.668548
Vig, I., Ács-Szabó, L., Benkő, Z., Poláková, S., Papp, L. A., Gregáň, J., & Miklós, I. G. (2025) · Cells · doi:10.3390/cells14211736
Lewis, A. G., Smith, J. R., Smardz, M., Sandoval, C. M., Suzuki, S. W., Bennett, B. D., & Gibney, P. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.06.687039
Fritsche, A.-P., Alasmari, A., Alshehri, M., Claverol, S., Fuller, H. R., McFarlane, R. J., & Hooks, M. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.02.691498
Alao, J. P., Islam, R. A., Toyoda, Y., Saitoh, S., & Rallis, C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.23.696270
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Kövér, B., Cohen, C. E., Seres, L., Raut, S., Ralser, M., Heineike, B. M., & Bähler, J. (2026) · Genetics · doi:10.1093/genetics/iyag064
Self-citationLim, K. K., Chung, J. J., Ma, S., Yen, C.-C., Zhang, L., & Chen, E. S. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27083410
Pongpom, M., Wattanasombat, S., Aphiwongcharoen, C., Limsamutpet, K., & Wangsanut, T. (2026) · ACS Omega · doi:10.1021/acsomega.6c00759
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Finkel, J. M., Williams, M. G., Nirmal, M. B., Pandey, S., Howe, E. D., Liu, C., Lohman, J. R., Sharma, N., & Vo, T. V. (2026) · Genes · doi:10.3390/genes17060606
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- Authors
- Rodríguez-López, M., Bordin, N., Lees, J., Scholes, H., Hassan, S., Saintain, Q., Kamrad, S., Orengo, C., & Bähler, J.
- Affiliations
- University College London, Institute of Healthy Ageing and Department of Genetics, Evolution & Environment
- Institute of Structural and Molecular Biology (GB)
- University College London, Institute of Structural and Molecular Biology
- University College London (GB)
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2023-10-03
- Volume
- 12
- ISSN
- 2050-084X (ISSN-L)
- OpenAlex
- W4387311335
- Cited by
- 18
- References
- 100
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 6
- FWCI
- 1.59
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Bristol Research (University of Bristol) (submittedVersion, cc-by)
- Explore Bristol Research (submittedVersion, cc-by)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/R009597/1)
- Newton-Moshara Fund (Scholarship)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- protein function prediction, Schizosaccharomyces pombe, deletion mutants, non-essential genes, oxidative stress resistance, guilt by association, gene ontology annotation, protein networks, protein homology, cellular aging, phenomics
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